The Roles of Hormone Signals Involved in Rhizosphere Pressure Response Induce Corm Expansion in Sagittaria trifolia

Abstract

Soil is the base for conventional plant growth. The rhizosphere pressure generated from soil compaction shows a dual effect on plant growth in agricultural production. Compacted soil leads to root growth stagnation and causes bending or thickening, thus affecting the growth of aboveground parts of plants. In arrowhead (Sagittaria trifolia L.), the corms derived from the expanded tips of underground stolons are its storage organ. We found that the formation of corms was significantly delayed under hydroponic conditions without rhizosphere pressure originating from soil/sand. In the initial stage of corm expansion, the anatomic structure of arrowhead corm-forming parts harvested from hydroponics and sand culture was observed, and we found that the corm expansion was derived from cell enlargement and starch accumulation. Comparative transcriptome analysis indicated that the corm expansion was closely related to the change in endogenous hormone levels. Endogenous abscisic acid and salicylic acid concentrations were significantly increased in sand-cultured corms. Higher ethylene and jasmonic acid contents were also detected in all arrowhead samples, demonstrating that these hormones may play potential roles in the rhizosphere pressure response and corm expansion. The expression of genes participating in hormone signaling could explain the rising accumulation of certain hormones. Our current results draw an extensive model to reveal the potential regulation mechanism of arrowhead corm expansion promoted by rhizosphere pressure, which will provide important references for further studying the molecular mechanism of rhizosphere pressure modulating the development of underground storage organs in other plants.

Keywords: corm expansion; plant hormone; rhizosphere pressure; transcriptome.

Figure 1

Morphological comparison of arrowheads in contrasting conditions. (a) Plant growth status of arrowheads 45 d after planting. l: leaf, ls: leafstalk, st: stolon, r: root, and c: corm. Bar represents 10 cm. (b–f) Plant height, root length, stolon length, stolon diameter, and corm diameter of two treatments 25 d and 45 d after planting. T and W represent sand culture and hydroponics, respectively. The error line indicates the standard deviation (SD) of multiple repeated samples. * means the significance of the difference between two treatments with Student’s t-test, ns: no significance, ** p < 0.01, **** p < 0.0001.

Figure 2

Anatomical structures of expanded and unexpanded arrowhead corm parts. Sampling time was 45 d after planting. T and W represent sand culture and hydroponics, respectively. ep: epidermis, pc: parenchyma cell, sg: starch granule; bar represents 100 μm.

Figure 3

Transcriptome identification. (a) Volcano map and quantity statistics of DEGs. (b) GO annotation of DEGs. (c) COG functional classification of DEGs. (d) Top 20 KEGG metabolic pathways of DEGs. The pathway circled in red box indicates that it is a significantly enriched pathway that we noticed.

Figure 4

Contents of hormones in two treatments at the initial stage of corm expansion. (a–g) Hormone contents of ABA (a), auxins (b), CKs (c), GA (d), ETH (e), JAs (f), and SA (g) in corms in contrasting conditions. The dashed boxes indicate the types covered by each hormone. T and W represent sand culture and hydroponics, respectively. Column heights indicate hormone contents. The error line indicates the standard deviation (SD) of three repeated samples. * means the significance of the difference between two treatments analyzed with Student’s t-test, ns: no significance, * p < 0.05, ** p < 0.01, *** p < 0.001, **** p < 0.0001.

Figure 5

Expression profiles of genes related to plant hormone metabolism in sand culture and hydroponics. Green, orange, and purple vertical lines indicate biosynthesis, degradation, and signaling genes, respectively (color figure online). The gene with a red dot behind it indicates that it is a differentially expressed gene (DEG). W1–3 and T1–3 represent three biological repeats in hydroponics and sand culture, respectively.

Figure 6

Relative expressions of ABA, JA, ETH, and SA metabolism-related genes in samples from sand culture and hydroponics. (a–d) Relative expressions of genes related to ABA (a), JA (b), ETH (c), and SA (d). Column height indicates gene expression level. T and W represent sand culture and hydroponics, respectively. The error line indicates the standard deviation (SD) of three replicates. * means the significance of the difference between two treatments analyzed with Student’s t-test, * p < 0.05, ** p < 0.01, *** p < 0.001, and **** p < 0.0001.

Figure 7

Model diagram of rhizosphere pressure response of arrowheads. In ‘hormone signaling’ the ‘?’ means that the interaction mechanism may exist, but not yet clear.